Reducing the genome size of organelles favours gene transfer to the nucleus

Selosse, Marc‐André; Albert, Béatrice; Godelle, Bernard

doi:10.1016/s0169-5347(00)02084-x

Cited by 129 publications

(91 citation statements)

References 49 publications

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“…This can lead to the nuclear gene either evolving a new function or becoming non-functional (i.e. a pseudogene) and finally erode [73]. If the gene product, however, -probably much more rarely -becomes targeted to its site of function, loss of either copy could be fixed by selection (or stochastically).…”

Section: A Mechanistic View On Gene Transfersmentioning

confidence: 99%

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Nowack

2014

Acta Soc Bot Pol

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The evolution of plastidsPrimary plastids, the photosynthetic organelles of Plantae (i.e. green algae/land plants, red algae, and glaucophytes) evolved more than 1 billion years ago (gya) through the endosymbiotic uptake of a cyanobacterium by a heterotrophic protist host [1][2][3]. Photosynthetic carbon fixation from the newly acquired plastid relieved the host from its dependency on the continuous uptake of organic carbon molecules from the environment. In addition to photosynthetic carbon fixation, plastids provide other beneficial metabolic functions to the plant/algal cell such as the assimilation of ammonia and sulfate into amino acids [4], assembly of iron-sulfur clusters [5], de novo biosynthesis of fatty acids [6], isopentenyl diphosphate (IPP) [7], and aromatic amino acids [8]; and they contribute to pathways that are distributed over several compartments, such as photorespiration and biosynthesis of pyrimidines and folates [9][10][11].Evolution of plastids was accompanied by a strong reduction of the size of the cyanobacterial genome and the transfer of thousands of cyanobacterial genes into the host nuclear genome, a process termed endosymbiotic gene transfer (EGT) [12,13]. This resulted in proteins localized to the cyanobacterium, now a full-fledged plastid, being synthesized in the cytoplasm and then imported into the plastid through a sophisticated import machinery (the TIC/ TOC complex; short for: translocon of the inner and outer chloroplast membranes) targeted by N-terminal transit peptides [14]. A multitude of solute transporters underlie the intricate metabolic crosstalk between plastid and the surrounding cell by controlling fluxes of metabolites and ions through the double membrane system that delimits the plastid [15][16][17]. Signaling pathways from and to the plastid communicate environmental cues and the metabolic and developmental status of different compartments within the plant/algal cell [18,19]. An interplay of eukaryote-and cyanobacterium-derived proteins coordinate plastid division with the host cell cycle [20].Following the establishment of primary plastids in Plantae, photosynthetic ability spread to other eukaryotic lineages through secondary endosymbioses [21,22]. In secondary endosymbioses a red or green alga served as an endosymbiont, leading to the establishment of secondary plastids in heterokontophytes (stramenopiles), cryptophytes, haptophytes, dinoflagellates, apicomplexa, chlorarachniophytes, and euglenophytes. In most cases the only remnant of the eukaryotic symbiont is one or two extra membranes that surround the secondary plastid. The nuclear genome of the * Email: e.nowack@uni-duesseldorf.deHandling Editor: Andrzej Bodył INVITED REVIEW Acta Soc Bot Pol 83(4): 387-397 DOI: 10.5586/asbp.2014.049 Received: 2014-11-16 Accepted: 2014-12-19 Published electronically: 2014 Paulinella chromatophora -rethinking the transition from endosymbiont to organelle Eva C.M. Nowack* Department of Biology, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf...

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Section: A Mechanistic View On Gene Transfersmentioning

confidence: 99%

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Nowack

2014

Acta Soc Bot Pol

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“…This dissimilarity in genome compactness cannot be explained by mutation rate differences because the estimated mutation rates in the two genetic compartments seem to be quite similar. Other factors that might explain this difference include a possible reduction in the power of random genetic drift in the mitochondrial compartment compared to the nuclear one as discussed by Lynch et al (2006) or selection for mitochondrial genome streamlining because of competition among mtDNA molecules for faster replication time (Selosse et al 2001).…”

Section: Trpmentioning

confidence: 99%

Mitochondrial Genome Sequence Evolution in Chlamydomonas

Popescu

Lee

2007

Genetics

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The mitochondrial genomes of the Chlorophyta exhibit significant diversity with respect to gene content and genome compactness; however, quantitative data on the rates of nucleotide substitution in mitochondrial DNA, which might help explain the origin of this diversity, are lacking. To gain insight into the evolutionary forces responsible for mitochondrial genome diversification, we sequenced to near completion the mitochondrial genome of the chlorophyte Chlamydomonas incerta, estimated the evolutionary divergence between Chlamydomonas reinhardtii and C. incerta mitochondrial protein-coding genes and rRNA-coding regions, and compared the relative evolutionary rates in mitochondrial and nuclear genes. Synonymous and nonsynonymous substitution rates do not differ significantly between the mitochondrial and nuclear protein-coding genes. The mitochondrial rRNA-coding regions, however, are evolving much faster than their nuclear counterparts, and this difference might be explained by relaxed functional constraints on the mitochondrial translational apparatus due to the small number of proteins synthesized in Chlamydomonas mitochondria. Substitution rates at synonymous sites in a nonstandard mitochondrial gene (rtl) and at intronic and synonymous sites in nuclear genes expressed at low levels suggest that the mutation rate is similar in these two genetic compartments. Potential evolutionary forces shaping mitochondrial genome evolution in Chlamydomonas are discussed.

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“…During evolution, organellar genomes have been partly reduced in size and DNA sequence fragments have been transferred to nucleus (Bensasson et al, 2001;Selosse et al, 2001). Some DNA sequences, referred to as 'promiscuous DNA' are still moving between these three genomes (Ellis, 1982).…”

Section: Introductionmentioning

confidence: 99%

Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization

2013

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We analysed the size, relative age and chromosomal localization of nuclear sequences of plastid and mitochondrial origin (NUPTs-nuclear plastid DNA and NUMTs-nuclear mitochondrial DNA) in six completely sequenced plant species. We found that the largest insertions showed lower divergence from organelle DNA than shorter insertions in all species, indicating their recent origin. The largest NUPT and NUMT insertions were localized in the vicinity of the centromeres in the small genomes of Arabidopsis and rice. They were also present in other chromosomal regions in the large genomes of soybean and maize. Localization of NUPTs and NUMTs correlated positively with distribution of transposable elements (TEs) in Arabidopsis and sorghum, negatively in grapevine and soybean, and did not correlate in rice or maize. We propose a model where new plastid and mitochondrial DNA sequences are inserted close to centromeres and are later fragmented by TE insertions and reshuffled away from the centromere or removed by ectopic recombination. The mode and tempo of TE dynamism determines the turnover of NUPTs and NUMTs resulting in their species-specific chromosomal distributions.

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Reducing the genome size of organelles favours gene transfer to the nucleus

Cited by 129 publications

References 49 publications

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Mitochondrial Genome Sequence Evolution in Chlamydomonas

Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization

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